TAXON 69 (1) • February 2020: 5–27 Nickrent • Parasitic angiosperms REVIEW Parasitic angiosperms: How often and how many? Daniel L. Nickrent Department of Plant Biology, Southern Illinois University, Carbondale, Illinois, 62901-6509, U.S.A. Address for correspondence: Daniel L. Nickrent, [email protected] DOI https://doi.org/10.1002/tax.12195 Abstract Angiosperms that morphologically and physiologically attach to other flowering plants by means of a haustorium have evolved 12 times independently resulting in 292 genera and ca. 4750 species. Although hemiparasites predominate, holoparasitism has evolved in all but two clades, Cassytha (Lauraceae) and Krameria (Krameriaceae). Santalales contains the largest number of gen- era (179) and species (2428) among the 12 parasitic plant lineages whereas Orobanchaceae is the largest single family with 102 genera and over 2100 species. This review presents the current state of knowledge on the molecular phylogenetic relationships among all clades of parasitic angiosperms. These methods have been particularly important in revealing the closest non-parasitic relatives of holoparasites, plants that exhibit reduced morphologies, increased substitution rates, and frequent horizontal gene transfers, all of which confound phylogenetics. Although comprehensive molecular phylogenies are still lacking for many of the large genera, nearly complete generic level sampling exists, thus allowing unprecedented understanding of the evolutionary relationships within and among these fascinating plants. Keywords classification; haustorium; molecular phylogenetics; parasitic plant Supporting Information may be found online in the Supporting Information section at the end of the article. ■ INTRODUCTION cultivated by humans (Nickrent & Musselman, 2016). In addi- tion to Orobanchaceae, Cuscuta L. (dodder, Convolvulaceae) Parasitic flowering plants, defined here as angiosperms (Dawson & al., 1994) and Arceuthobium M.Bieb. (dwarf mis- that attach to host plants by means of haustoria, continue to tletoe, Viscaceae) (Hawksworth & Wiens, 1996) impact agri- attract attention among scientists in myriad disciplines. culture and forestry, respectively. Most of the remaining Interest in parasitic plants has increased over the past three genera comprise species that not only do not damage crops decades as documented by membership in the International but are in fact keystone components of natural ecosystems Parasitic Plant Society, attendance at their biennial meetings, (Watson, 2001, 2009). These plant parasites have positive and number of publications relating to this subject. Discov- interrelationships with other species in the community by eries about these plants are increasing at a rapid pace, partic- influencing competition, nutrient cycling, and community ularly with Orobanchaceae where physiological, genomic biodiversity (Press & Phoenix, 2005; Bardgett & al., 2006; and biochemical work has elucidated the details of host rec- Hatcher & al., 2012). Molecular methods have revealed previ- ognition, haustorium formation, and attachment. Only rela- ously unknown phenomena, e.g., floral development in Raf- tively recently have strigolactones been recognized as flesia R.Br., the largest flower in angiosperms (Nikolov germination stimulants (Matusova & al., 2005; Wang & al., 2013), increased evolutionary rates (Bromham & al., & Bouwmeester, 2018) and these molecules have since 2013), horizontal gene transfer (Yang & al., 2016), and chlo- gained increased importance not only in parasitic plants roplast genome (plastome) reduction (Wicke & al., 2013; Su but also non-parasites as they represent a new category of & al., 2019). plant growth regulators (Zwanenburg & Blanco-Ania, In addition to the above areas, molecular phylogenetic 2018) and participate in the establishment of arbuscular methods have been used to address a number of long-standing mycorrhizae (Gough & Bécard, 2016; Luginbuehl & Old- issues in parasitic plant taxonomy and evolutionary biology. royd, 2016). The vast majority of the current literature on Indeed, it is no exaggeration to say that these methods have parasitic plants involves two genera: Orobanche L. and revolutionized our understanding of parasitic plant relation- Striga Lour. (Orobanchaceae) owing to their importance as ships. This is especially true for those clades with members pathogens of crops (Joel & al., 2013). that are holoparasitic (non-photosynthetic) where morpholog- Although 292 genera and ca. 4750 species of flowering ical modifications (especially reductions) provide few clues as plants are parasitic, only about 25 genera are considered path- to their affinity. As shown below, molecular methods, at all ogens owing to their negative impact upon host plants levels of the taxonomic hierarchy, have been effective in Article history: Received: 10 May 2019 | returned for (first) revision: 20 Sep 2019 | (last) revision received: 25 Oct 2019 | accepted: 30 Oct 2019 | published online: 17 Mar 2020 | Associate Editor: Joachim W. Kadereit | © 2020 International Association for Plant Taxonomy Version of Record 5 Nickrent • Parasitic angiosperms TAXON 69 (1) • February 2020: 5–27 Fig. 1. Representative members of the 12 clades of angiosperm haustorial parasites. Letters A–L correspond to the clades shown in Fig. 2. A, Cassytha filiformis (South Africa); B, Hydnora africana (South Africa); C, Cynomorium coccineum (Spain); D, Krameria ixine (Puerto Rico); E, Rafflesia pricei (Malaysia); F, Pilostyles thurberi (U.S.A.); G, Cytinus ruber (France); H, Amyema artensis (Papua New Guinea); I, Mitrastemon yamamotoi (Japan); J, Pholisma culiacanum (Mexico); K, Cuscuta rostrata (U.S.A.); L, Harveya purpurea (South Africa). — All photos by D.L. Nickrent except G (W. Meijer), I (M. Satou), and K (O. Linares). resolving relationships, thus providing the basis for develop- because both groups are heterotrophic, deriving their nutri- ing modern classifications. ents from another plant. An important distinction, however, is that haustorial parasites feed directly on another plant via modified roots (rarely shoots or leaves) called the hausto- ■ WHAT IS A PARASITIC PLANT? rium; in contrast mycoheterotrophs obtain their nutrition indirectly from another plant via a mycorrhizal fungus. Indeed the concept of what exactly constitutes a para- The mycorrhizal fungus, attached to the roots of a photosyn- sitic angiosperm has in recent years been somewhat con- thetic plant, thus acts as a bridge between that plant and the fused. This stems from whether one takes a functional or mycoheterotroph, such that nutrients (carbon) flow from structural perspective. In this paper, two types of heterotro- plant root, to mycorrhizal fungus and then to the mycohetero- phic angiosperms that derive nutrients from another plant troph. These plants may also be called mycoheterotrophic will be recognized: mycoheterotrophs and haustorial para- epiparasites or ectomycorrhizal epiparasites because they sites. Although phylogenetically distinct, these two types are epiparasitic on the fungus. Mycoheterotrophs occur in of heterotrophs share a number of physiological, anatomi- 10 angiosperm families including monocots and eudicots cal, developmental, and life history similarities. Some (Soltis & al., 2018: table 13.3). To avoid confusion, the choose to call all of these “parasitic plants” (e.g., https:// terms parasite or parasitic plant here refers to haustorial par- botany.org/Parasitic_Plants/), and in one sense this is true asites, and examples of all lineages are shown in Fig. 1. Both 6 Version of Record TAXON 69 (1) • February 2020: 5–27 Nickrent • Parasitic angiosperms parasites and mycoheterotrophs have mixotrophic (combina- the phylogenetic tree published by Nickrent & al. (2005) tion of autotrophic and heterotrophic feeding) and fully- where Dactylanthus Hook.f., Hachettea Baill., and Mystrope- heterotrophic (non-photosynthetic) representatives. Finally, talon Harv. were sister to three Santalales genera (their fig. 2) mycoheterotrophs are sometimes mistakenly called sapro- or as a clade within Santalales (their fig. 3). Evidence support- phytes (Soltis & al., 2018: table 13.1). There are no true sap- ing an internal position was provided first in a conference rophytes in the angiosperms; only fungi can directly utilize abstract (Su & Hu, 2008) and later published by Su & al. dead organic material. (2012), who used five nuclear and one mitochondrial gene in phylogenetic analyses with several genera in Santalales. The internal positions of Balanophoraceae s.l. (including ■ HOW OFTEN HAS PARASITISM EVOLVED Mystropetalaceae, see below) were confirmed in the compre- IN ANGIOSPERMS? hensive analysis of Su & al. (2015). The uncertainty about Balanophoraceae s.l. and Santalales also prevented others Many publications introduce the subject of parasitic (e.g., Barkman & al., 2007; Naumann & al., 2013) from con- angiosperms by citing figures on the number of different fidently stating the number of origins of parasitism in angio- lineages that exist or how many times haustorial parasites sperms. Bromham & al. (2013) showed that parasitic plants have evolved. More often than not, the numbers that are have increased substitution rates in all three subcellular given indicate uncertainty or erroneous/outdated informa- genomes and correctly identified the 12 independent evolu- tion. Identifying the closest non-parasitic relatives of para- tionary origins, including the association of Balanophoraceae sitic plants originated with traditional,